Abstract
Colistin resistance by mobilisable mcr genes has been described in bacteria of food-animal origin worldwide, which has raised public health concerns about its potential foodborne transmission to human pathogenic bacteria. Here we provide baseline information on the molecular epidemiology of colistin-resistant, mcr-positive Escherichia coli and Salmonella isolates in food-producing animals in Italy in 2014-2015. A total 678, 861 and 236 indicator E. coli, Extended Spectrum Beta-Lactamase (ESBL)/AmpC-producing E. coli, and Salmonella isolates, respectively, were tested for colistin susceptibility. These isolates were collected according to the EU harmonized antimicrobial resistance monitoring program and are representative of at least 90 and 80% of the Italian poultry (broiler chickens and turkeys) and livestock (pigs and bovines < 12 months) production, respectively. Whole genome sequencing by Illumina technology and bioinformatics (Center for Genomic Epidemiology pipeline) were used to type 42 mcr-positive isolates by PCR. Colistin resistance was mainly observed in the ESBL/AmpC E. coli population, and was present in 25.9, 5.3, 6.5, and 3.9% of such isolates in turkeys, broilers, pigs, and bovines, respectively. Most colistin-resistant isolates (141/161, 87.5%) harbored genes of the mcr-1 group. mcr-1 was also detected in a small proportion of Salmonella isolates (3/146, 2.0%) in turkeys. Additional mcr types were mcr-3 in four ESBL-producing E. coli from bovines, and two mcr-4 in ESBL (n = 1) and indicator E. coli (n = 1) from pigs and bovines. We describe notable diversity of mcr variants with predominance of mcr-1.1 and mcr-1.2 on conjugative IncX4 plasmids in E. coli and in Salmonella serovars Typhimurium, Newport, Blockley from turkey. A new variant, mcr-1.13 was detected in the chromosome in E. coli in turkey and pig isolates. Additionally, we describe mcr-3.2 and mcr-4.3 in E. coli from bovines, and mcr-4.2 in E. coli from pigs. These findings elucidate the epidemiology of colistin resistance in food-producing animals in Italy along with its genetic background, and highlight the likelihood of mcr horizontal transfer between commensal bacteria and major food-borne pathogens (Salmonella) within the same type of productions. Thorough action and strategies are needed in order to mitigate the risk of mcr transfer to humans, in a “One Health” perspective.
Highlights
Colistin is a polymyxin classified among the Highest Priority Critically Important Antimicrobials for human medicine by the World Health Organization (WHO), and it is considered a last resort antimicrobial for the treatment of infections by carbapenem-resistant Enterobacteriaceae in humans (Poirel et al, 2017).In 2015, colistin resistance mediated by mcr-1, a phosphoethanolamine transferase gene located on a transferable plasmid was first reported in Escherichia coli from animals, food and patients from China (Liu et al, 2016)
In 2014, colistin resistance was detected in 25.9% (58/224) and 5.3% (13/244) of the Extended Spectrum Beta-Lactamase (ESBL)/AmpC-producing E. coli from fattening turkeys and broilers, respectively
A similar prevalence was observed among the indicator commensal E. coli, with colistin resistance occurring in 22.9% (39/170) and 5.9% (9/170) of isolates from turkeys and broilers, respectively (Table 1)
Summary
In 2015, colistin resistance mediated by mcr-1, a phosphoethanolamine transferase gene located on a transferable plasmid was first reported in Escherichia coli from animals, food and patients from China (Liu et al, 2016). At least 32 countries from the five continents have found mcr-1 in E. coli isolates from different sources including humans, animals and foods (Xavier et al, 2016). In Europe, the presence of mcr-1 was first detected in E. coli from poultry meat and humans in Denmark (Hasman et al, 2015). This gene was found in Enterobacteriaceae from different sources in almost all European countries, including Italy (Battisti, 2016; Cannatelli et al, 2016). In 2016, a new mcr gene, mcr-2, was described in E. coli in calves and piglets in Belgium (Xavier et al, 2016), followed by the description of three additional mobile colistin resistance genes in 2017, namely mcr-3 (Yin et al, 2017) in E. coli isolated from pig in China, mcr-4 (Carattoli et al, 2017) in Salmonella and E. coli from pigs in Italy, Spain and Belgium, and mcr-5 (Borowiak et al, 2017) in Salmonella Paratyphi B from poultry and environmental sources from Germany
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